Vagus Motor Neuron Topographic Map Determined by Parallel Mechanisms of hox5 Expression and Time of Axon Initiation

Gabrielle R. Barsh, Adam J. Isabella, Cecilia B. Moens

Research output: Contribution to journalArticlepeer-review

24 Scopus citations

Abstract

Many networks throughout the nervous system are organized into topographic maps, where the positions of neuron cell bodies in the projecting field correspond with the positions of their axons in the target field. Previous studies of topographic map development show evidence for spatial patterning mechanisms, in which molecular determinants expressed across the projecting and target fields are matched directly in a point-to-point mapping process. Here, we describe a novel temporal mechanism of topographic map formation that depends on spatially regulated differences in the timing of axon outgrowth and functions in parallel with spatial point-to-point mapping mechanisms. We focus on the vagus motor neurons, which are topographically arranged in both mammals and fish. We show that cell position along the anterior-posterior axis of hindbrain rhombomere 8 determines expression of hox5 genes, which are expressed in posterior, but not anterior, vagus motor neurons. Using live imaging and transplantation in zebrafish embryos, we additionally reveal that axon initiation is delayed in posterior vagus motor neurons independent of neuron birth time. We show that hox5 expression directs topographic mapping without affecting time of axon outgrowth and that time of axon outgrowth directs topographic mapping without affecting hox5 expression. The vagus motor neuron topographic map is therefore determined by two mechanisms that act in parallel: a hox5-dependent spatial mechanism akin to classic mechanisms of topographic map formation and a novel axon outgrowth-dependent temporal mechanism in which time of axon formation is spatially regulated to direct axon targeting. The development of topographic maps classically relies upon spatial patterning mechanisms. Barsh et al. show that in zebrafish vagus motor neurons, map formation is determined by a hox5-dependent spatial mechanism that acts in parallel with a novel temporal mechanism dependent upon the time of axon outgrowth.

Original languageEnglish (US)
Pages (from-to)3812-3825.e3
JournalCurrent Biology
Volume27
Issue number24
DOIs
StatePublished - Dec 18 2017
Externally publishedYes

Bibliographical note

Publisher Copyright:
© 2017 Elsevier Ltd

Keywords

  • axogenesis
  • axon initiation
  • branchiomotor neuron
  • hoxa5
  • hoxb5
  • topographic map
  • vagus
  • vagus motor neuron
  • zebrafish

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